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Science 297 (5579): 259-263

Copyright © 2002 by the American Association for the Advancement of Science

Mediation of Poly(ADP-Ribose) Polymerase-1-Dependent Cell Death by Apoptosis-Inducing Factor

Seong-Woon Yu,1* Hongmin Wang,1* Marc F. Poitras,1 Carmen Coombs,1 William J. Bowers,5 Howard J. Federoff,5 Guy G. Poirier,6 Ted M. Dawson,124 Valina L. Dawson1234dagger

Poly(ADP-ribose) polymerase-1 (PARP-1) protects the genome by functioning in the DNA damage surveillance network. PARP-1 is also a mediator of cell death after ischemia-reperfusion injury, glutamate excitotoxicity, and various inflammatory processes. We show that PARP-1 activation is required for translocation of apoptosis-inducing factor (AIF) from the mitochondria to the nucleus and that AIF is necessary for PARP-1-dependent cell death. N-methyl-N'-nitro-N-nitrosoguanidine, H2O2, and N-methyl-D-aspartate induce AIF translocation and cell death, which is prevented by PARP inhibitors or genetic knockout of PARP-1, but is caspase independent. Microinjection of an antibody to AIF protects against PARP-1-dependent cytotoxicity. These data support a model in which PARP-1 activation signals AIF release from mitochondria, resulting in a caspase-independent pathway of programmed cell death.

1 Departments of Neurology,
2 Neuroscience, and
3 Physiology; and
4 the Institute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA.
5 Department of Neurology, Center for Aging and Developmental Biology, University of Rochester, NY 14642, USA.
6 Health and Environment Unit, Laval University Medical Research Center, CHUQ, Ste-Foy, Quebec G1V 4G2, Canada.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed. E-mail: vdawson{at}

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X. Wang, S. Zhu, Z. Pei, M. Drozda, I. G. Stavrovskaya, S. J. Del Signore, K. Cormier, E. M. Shimony, H. Wang, R. J. Ferrante, et al. (2008)
J. Neurosci. 28, 9473-9485
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Cellular NAD Replenishment Confers Marked Neuroprotection Against Ischemic Cell Death: Role of Enhanced DNA Repair.
S. Wang, Z. Xing, P. S. Vosler, H. Yin, W. Li, F. Zhang, A. P. Signore, R. A. Stetler, Y. Gao, and J. Chen (2008)
Stroke 39, 2587-2595
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CCCTC-binding Factor Activates PARP-1 Affecting DNA Methylation Machinery.
T. Guastafierro, B. Cecchinelli, M. Zampieri, A. Reale, G. Riggio, O. Sthandier, G. Zupi, L. Calabrese, and P. Caiafa (2008)
J. Biol. Chem. 283, 21873-21880
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Japanese encephalitis virus infection activates caspase-8 and -9 in a FADD-independent and mitochondrion-dependent manner.
C.-H. Tsao, H.-L. Su, Y.-L. Lin, H.-P. Yu, S.-M. Kuo, C.-I Shen, C.-W. Chen, and C.-L. Liao (2008)
J. Gen. Virol. 89, 1930-1941
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Bobel-24 and Derivatives Induce Caspase-Independent Death in Pancreatic Cancer Regardless of Apoptotic Resistance.
M. Parreno, I. Casanova, M. V. Cespedes, J. P. Vaque, M. A. Pavon, J. Leon, and R. Mangues (2008)
Cancer Res. 68, 6313-6323
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Interaction of Heterogeneous Nuclear Ribonucleoprotein C1/C2 with a Novel cis-Regulatory Element within p53 mRNA as a Response to Cytostatic Drug Treatment.
K. J. Christian, M. A. Lang, and F. Raffalli-Mathieu (2008)
Mol. Pharmacol. 73, 1558-1567
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Glioma Regression In vitro and In vivo by a Suicide Combined Treatment.
V. Garcia-Escudero, R. Gargini, and M. Izquierdo (2008)
Mol. Cancer Res. 6, 407-417
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The microtubule-targeting agent CA4P regresses leukemic xenografts by disrupting interaction with vascular cells and mitochondrial-dependent cell death.
I. Petit, M. A. Karajannis, L. Vincent, L. Young, J. Butler, A. T. Hooper, K. Shido, H. Steller, D. J. Chaplin, E. Feldman, et al. (2008)
Blood 111, 1951-1961
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Gender-Related Differences in Apoptotic Pathways After Neonatal Cerebral Ischemia.
S. Renolleau, S. Fau, and C. Charriaut-Marlangue (2008)
Neuroscientist 14, 46-52
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Advances in Neuronal Cell Death 2007.
M. M. Harraz, T. M. Dawson, and V. L. Dawson (2008)
Stroke 39, 286-288
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Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs.
S. Oka, M. Ohno, D. Tsuchimoto, K. Sakumi, M. Furuichi, and Y. Nakabeppu (2008)
EMBO J. 27, 421-432
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Functional Localization of Two Poly(ADP-Ribose)-Degrading Enzymes to the Mitochondrial Matrix.
M. Niere, S. Kernstock, F. Koch-Nolte, and M. Ziegler (2008)
Mol. Cell. Biol. 28, 814-824
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Apoptosis-Inducing Factor Is a Target for Ubiquitination through Interaction with XIAP.
J. C. Wilkinson, A. S. Wilkinson, S. Galban, R. A. Csomos, and C. S. Duckett (2008)
Mol. Cell. Biol. 28, 237-247
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Quantitative analysis of the binding affinity of poly(ADP-ribose) to specific binding proteins as a function of chain length.
J. Fahrer, R. Kranaster, M. Altmeyer, A. Marx, and A. Burkle (2007)
Nucleic Acids Res. 35, e143
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Ca2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity.
Y. Duan, R. A. Gross, and S.-S. Sheu (2007)
J. Physiol. 585, 741-758
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Poly(ADP-ribosyl)ation in mammalian ageing.
S. Beneke and A. Burkle (2007)
Nucleic Acids Res. 35, 7456-7465
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